A stepwise route to domesticate rice by controlling seed shattering and panicle shape

Significance

Rice is one of the most important crops worldwide. Loss of seed shattering in domesticated rice, previously attributed to single-gene mutations such as sh4, is reported to be the essential genetic change resulting in yield increases during domestication. However, we show that sh4 alone is insufficient, and other genes, such as qSH3, are required to cause abscission layer disruption. The evolution of non-seed-shattering behavior therefore required multiple mutations. Furthermore, shattering loss in the genetic background of wild rice does not increase yield. We demonstrate that closed panicle formation controlled by SPR3 both increases yield and facilitates recruitment of sh4 and qSH3, which synergistically augment yield, leading to a stepwise model for rice domestication.

Abstract

Asian rice ( Oryza sativa L.) is consumed by more than half of the world's population. Despite its global importance, the process of early rice domestication remains unclear. During domestication, wild rice ( Oryza rufipogon Griff.) acquired non-seed-shattering behavior, allowing humans to increase grain yield. Previous studies argued that a reduction in seed shattering triggered by the sh4 mutation led to increased yield during rice domestication, but our experiments using wild introgression lines show that the domesticated sh4 allele alone is insufficient for shattering loss in O. rufipogon. The interruption of abscission layer formation requires both sh4 and qSH3 mutations, demonstrating that the selection of shattering loss in wild rice was not as simple as previously suggested. Here we identified a causal single-nucleotide polymorphism at qSH3 within the seed-shattering gene OsSh1, which is conserved in indica and japonica subspecies but absent in the circum-aus group of rice. Through harvest experiments, we further demonstrated that seed shattering alone did not significantly impact yield; rather, yield increases were observed with closed panicle formation controlled by SPR3 and further augmented by nonshattering, conferred by integration of sh4 and qSH3 alleles. Complementary manipulation of panicle shape and seed shattering results in a mechanically stable panicle structure. We propose a stepwise route for the earliest phase of rice domestication, wherein selection of visible SPR3-controlled closed panicle morphology was instrumental in the sequential recruitment of sh4 and qSH3, which together led to the loss of shattering.